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ISSN (Print) 0023-4001 ISSN (Online) 1738-0006

Korean J Parasitol Vol. 56, No. 3: 215-227, June 2018 ▣ MINI REVIEW https://doi.org/10.3347/kjp.2018.56.3.215

An Overview of -borne Nematodiases among Returned Travelers for Recent 25 Years– Unexpected Diseases Sometimes Far Away from the Origin

1,2 3,4 5 6, Jorge Costa Eiras , Gilberto Cezar Pavanelli , Ricardo Massato Takemoto , Yukifumi Nawa * 1Departamento de Biologia, Faculdade de Ciências, Universidade do Porto, Rua do Campo Alegre, Edifício FC4, 4169-007 Porto, Portugal; 2Centro Interdisciplinar de Investigação Marinha e Ambiental (CIIMAR/CIMAR), Terminal de Cruzeiros do Porto de Leixões, Av. General Norton de Matos, 4450-308 Matosinhos, Portugal; 3Unicesumar, Programa de pós-graduação em Promoção da Saúde, Bloco 7, Avenida Guerner Dias, 1610-Jardim Aclimação, Maringá-PR, 87050-900, Brasil; 4Pesquisador do Instituto Cesumar de Ciência, Tecnologia e Inovação, Bloco 11-50 andar (44) 3027- 6360 Ramal 1346, Brasil; 5UEM, Nupelia, Bloco G90, Av. Colombo, 5790-zona 7, Maringá-PR, CEP 87020-900, Brasil; 6Tropical Diseases Research Center, Faculty of Medicine, Khon Kaen University, 123 Mitrapap Highway, Khon Kaen 40002,

Abstract: Along with globalization of traveling and trading, fish-borne nematodiases seems to be increasing in number. However, apart from occasional and sporadic case reports or mini-reviews of particular diseases in particular countries, an overview of fish-borne nematodiasis among travelers have never been performed. In this review, we gathered fish- borne nematodiasis among travelers for recent 25 years by an extensive global literature survey using appropriate key- words, e.g. travelers diseases, , anisakiasis, , , sushi, sashimi, ceviche, Gna- thostoma, Pseudoterranova, , Capillaria, etc., as well as various combinations of these key words. The Internet search engines PubMed, Medline, Google and Googler Scholar were used as much as possible, and the references of every paper were checked in order to identify useful and reliable publications. The results showed unexpectedly high inci- dence of gnathostomiasis and low incidence of anisakidosis. The different incidence values of the infection with several fish-borne zoonotic species are discussed, as well as some epidemiological aspects of the . The dif- ficulties of differential diagnosis in non-endemic countries are emphasized. It is concluded that travelers must avoid risky behaviors which can lead to infection and that physicians and health authorities must advice travelers on the risks of eat- ing behaviors during travel.

Key words: Fish-borne nematode, , human infection, public health, traveler

INTRODUCTION these problems [2-4], the number of cases of imported infec- tious diseases has been rather increasing with time. Traveling abroad is nowadays very frequent and the number Travelers are accidentally infected with fish-borne parasites. of people involved increased drastically in the last years. Accord- The contact with new ethnic dishes, the novelty of a different ing to the World Tourism Organization destinations around the way of “cooking” in the so-called exotic countries, are factors world welcomed 956 million international tourists from Janu- leading people to try different kind of which may cause ary to September 2016 [1]. Most of these people probably ex- infection with various nematode species. The symptoms of the pose themselves to a wide range of pathogens, including hel- infection can appear almost immediately or later, sometimes minth parasites, or adopt some risky behaviors favoring the in- after having returned home. Therefore, the incidence and geo- fection with a wide variety of pathogens. In spite of extensive re- graphic range of certain fish-borne parasitic diseases may in- views and alerts about the risk factors for travelers involved in crease and constitute emerging zoonotic helminth infections- infections that have newly appeared in a population or have

Received 25 January 2018, revised 6 May 2018, accepted 14 May 2018. existed but are rapidly increasing in incidence or geographic • Corresponding author ([email protected]) * range [2]. © 2018, Korean Society for Parasitology and Tropical Medicine A number of studies have been made about zoonotic fish- This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) borne nematodiases among returned travelers. Most of them which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. are simple case reports [5-10]. Several researchers produced re-

215 216 Korean J Parasitol Vol. 56, No. 3: 215-227, June 2018

views on a particular parasite like spp. [11-20], or snails and rarely shrimps [37], a case was reported to have oc- Capillaria philippinensis [21,22] where the infection of travelers curred after eating uncooked fish [38]. is referred to in a particular country or region. As far as the au- In some Asian countries there is a strong tradition of eating thors are aware there are only 3 studies reporting all the cases raw or undercooked fish prepared in several ways. In addition to of ocular gnathostomiasis all over the world between 1937 globally known “Sushi” and “Sashimi” in [12], similar and 2005 [23], and till 2010 [18] and further updated untill habits like “Koi pla”, “Pla ra”, “Pla som” and “Som fak” in 2017 [24]. Clément-Rigolet et al. [15] presented a list of im- Thailand [39] are present in Laos and Cambodia. In the Philip- ported gnathostomiasis to western countries (immigrants and pines, “Kinilaw”, “Sabaw” and “Sukba” are known as the tradi- travelers) since 1980 by chronological order of the reports, list- tional food habits, which enable fish-borne zoonotic parasite in- ing 42 cases. fections. Moreover, there are a number of other different ways of However, a world survey of fish-borne nematodiases among preparing raw fish in other countries like “Ceviche” in , returned travelers has never been conducted. In this review, the “Gravlax” in Nordic countries, “Boquerones in vinegar” in Spain, authors report the world known cases of human fish-borne or “Crudo” in Italy. These dishes, especially Japanese “Sushi”, are nematodiases among returned travelers, in a tabulated form, very popular in their original country, and actually a number of indicating for each parasite species, the country of infection, them and imitated ones have been spreading all over the world the country of the returned traveler, the number of cases and where they constitute a kind of “fashionable” healthy food and the references. A general discussion is provided on the differ- now has become a strong risk of acquiring fish-borne nematodi- ent aspects of this interesting problem. ases [12]. In addition to the cultural changes of eating habits, in- crease of global trading and traveling, expansion of fishing areas FISH-BORNE PARASITIC ZOONOSES and development of cold transportation systems caused consid- erable changes in epidemiology of fish-borne parasitic zoonoses Fish-borne parasitic zoonoses is a major and important part [40-44]. of food-borne parasitic zoonoses. More than 10 years ago, Chai et al. [25] wrote an excellent review on this topic, and the Anisakidosis review was further expanded as a monograph entitled “Food- Anisakidosis is the most representative fish-borne nematodia- Borne Parasitic Zoonoses: Fish and Plant-Borne Parasites” by sis with approximately 20,000 reported worldwide of which Murrell et al. [26]. Among fish-borne parasitic zoonoses, >90% were from Japan and most other cases from coastal Eu- much attentions and efforts have been directed towards fish- rope (Netherlands, Germany, France and Spain), USA (west borne , especially of small fluke infections [27- coast and Hawaii in particular) [45]. Most cases of human infec- 29], but not directed against nematodiases. may be tions are caused by Anisakis simplex, A. physeteris and Pseudoter- infected with fish-borne if the fish are eaten alive, ranova decipiens (previously known as Phocanema decipiens) and raw or undercooked. For some nematode species, the parasites far less frequently by other members of the family Anisakidae may be ingested when people eat raw meat of mammals, such as Anisakis pegreffii, Contracaecum species, Hysterothylacium , amphibians and reptiles, which may be involved as in- species, Raphidascaris species and Thynnascaris species [45,46]. termediate or paratenic hosts in the life cycle of the fish-borne Anisakis pegreffii is a sibling species of A. simplex. Recently, the eti- nematodes. The fish-borne nematodes most frequently found ologic agents of human anisakiasis in Korea, which were mor- in humans are the members of Anisakidae, i.e., Anisakis spp. phologically Anisakis type I larvae, were molecularly confirmed [30] and Pseudoterranova spp. [31], followed by the Gnathosto- to be A. pegreffii larvae [47,48]. Moreover, most of the Anisakis matidae Gnathostoma spp. [12], and Capillaria philippinensis type I larvae detected in 7 fish species from the Yellow Sea and [21]. Some other species such as Hysterothylacium aduncum the South Sea in Korea were also identified as A. pegreffii [49]. [32,33], Contracaecum spp. [34], Eustrongylides spp. [35], Dioc- The term anisakidosis refers to disease caused by any mem- tophyme renale [36] are also known as fish-borne zoonotic ber of the family Anisakidae, whereas anisakiasis is caused by pathogens in humans, but their infections are very rarely re- members of the genus Anisakis and pseudoterranovosis by the ported than those of the afore-mentioned species. Although A. genus Pseudoterranova [46]. cantonensis infection in humans can occur by consuming land- In relation to the traditional custom of eating “Sushi” and Eiras et al.: Fish-borne nematodiases among returned travelers 217

“Sashimi”, anisakidosis is still a public health issue in Japan woman in Dubai, UAE [81]; one case of Columbian cocaine [50,51]. Along with the global popularization of “Sushi” and dealer arrived at Madrid, Spain [82]. “Sashimi”, cases have been reported from unexpected coun- tries like Australia [34], Austria [52], Brazil [53], Germany [54] Gnathostomiasis etc. In particular, anisakidosis is an emerging public health of Gnathostomiasis is one of the typical fish-borne nematodia- Korea [55,56]. Anisakidosis due to Pseudoterranova sp. infec- ses caused by eating raw or undercooked fish meat containing tion is emerging in Chile [57-59] and Peru [60,61]. infective third stage larvae. The disease has long been known Apart from direct mechanical and chemical damages of gas- to be endemic in Northeast to Southeast , especially Thai- trointestinal mucosa by anisakid larvae, recently antigenic land and Japan [83]. Since 1970, outbreaks of this disease components of anisakid larvae are proven to cause food aller- have been reported from , mostly from Mexico gy and gastrointestinal allergy [45,46,62,63]. Thus, pathogene- and Ecuador [84,85]. Gnathostoma spp. are apparently the sis of anisakid parasites may be much more complicated than most common fish-borne nematodes found among travelers. we thought. is endemic in the Southeast and East Asia whereas G. binucleatum is endemic in some Latin Ameri- can countries (Mexico, Ecuador and Peru), and in some coun- Intestinal capillariasis is a disease caused by an auto-infec- tries the disease is considered a public health problem [84], tion of the intestinal nematode, Capillaria philippinensis. Hu- namely in Mexico where over 10,000 cases of the illness were man infection occurs by ingesting freshwater or brackish water reported by 2010 [85]. Humans can be infected by ingesting fish harboring the infective stage larve of this parasite. The en- raw or poorly cooked fish, , , and some mammals demic of this disease was first found in northern Luzon of the which have the advanced third stage larvae and constitute sec- Philippines [21] and then central to northeast Thailand [64]. ond intermediate or paratenic . Some people are infected In Egypt, the first case was found in Cairo [65] and the parasite by ingesting live fish – some Japanese people enjoy swallow- is now established and spread to the Upper Egypt [66]. In Tai- ing live in drinking whisky or Japanese rice wine. Sev- wan, the first case was reported by Hwang et al. [67], and since eral human infections due to this behavior were described then, a total of 30 cases have been recorded, mostly among 2 [86]. Apparently Gnathostoma spp. may be found in any fish Taiwanese aboriginal tribes, suggesting that C. philippinensis species, and the worms have been collected from a number of has established in Taiwan [68]. Among those 30 cases, 5 cases different freshwater and brackish water fish specimens. Anoth- have a history of traveling either to the Philippines (2 cases) er way of contamination is drinking water containing crusta- and/or Thailand (4 cases). In addition to those endemic coun- ceans () which serve as intermediate hosts [87,88]. The tries, sporadic cases have been reported from several Asian infection can also be contracted by the penetration of of countries; the first case in was recently recorded in the food handlers by the nematodes larvae in infected meat or use Hainan Island [69]. Three sporadic cases without international of contaminated meat as poultice [89]. travel history have been reported in [70]. In Japan, 6 cas- es including 1 Japanese traveler returned from Malaysia and Eustrongylides and Dioctophyma renale Singapore [71] and 1 Thai immigrant worker [72], have been Eustrongylides is, together with other 2 genera, Hystrichis and reported. In Korea, 7 cases have been reported including 3 in- Dioctophyma, constituting of the fish-borne nematode Family digenous [73-75] and 4 cases of possible overseas infection. Dioctophymatidae. While Hystrichis and Eustrongylides are nat- Among 4 cases of overseas infection, 2 cases were in Saipan urally intestinal parasites of fish-eating birds, Dioctophyma is a (one Korean resident in Saipan [76] and one Korean traveler parasite of mammals infecting in the kidney [90]. Until recent to Saipan [77]) and 1 case each of a temporary resident in In- discovery of a female Eustrongylides worm from the lower limb donesia [74] and the Philippines [78]. Three cases were report- skin in Sudan [35], all 5 cases of Eustrongylides infection in hu- ed also from Lao PDR [79], 2 of which were the seasonal mi- mans were reported from USA with the recovery of a larval grant workers returned from the endemic area of Thailand. stage worm from the peritoneal cavity [91-95]. Dioctophyma re- One case each was reported from various countries; from Iran nale infection in humans is also extremely rare. When Beaver [80]; from Italy infected in Indonesia [5]; 1 case of Egyptian and Theis (1979) discovered the first human case of subcuta- 218 Korean J Parasitol Vol. 56, No. 3: 215-227, June 2018

neous nodular lesion by a D. renale [96], they have made indicated-only one case which no doubt could be considered an extensive literature review on all previously reported D. re- a traveler was included in the present paper. In the study of ill- nale infection in humans and listed 13 cases, all of which were ness among travelers returned to France from the tropics, An- the kidney/urinary tract involvement with mature adult worms sart et al. [112,113] referred the occurrence of several cases of [96]. Since then, several sporadic case reports have been ap- gnathostomiasis. However, the countries visited were not de- peared in the literature until the most recent case from Iran tailed, neither the kind of traveler (tourist or immigrant, etc.). [97]. Although several case report papers referred that over 20 For these reasons those cases are not included in the present cases of D. renale infection in humans have been reported study. Similarly, a case of intestinal capillariasis detected in a [98,99], the exact number of cases have not been determined. Colombian man in Spain described by Dronda et al. [82] was Now we are conducting an extensive literature survey on Dioc- not considered because of the unclearness of the travel history tophyma renale infection in humans and found a total of more of the patient. In the literature survey we found 3 cases of trav- than 40 cases [Nawa et al. manuscript in preparation]. elers infected with fish-borne nematodes but, acquired the dis- ease by ingesting other hosts than fish (frogs, boar, duck, DATA COLLECTION AND THE CRITERIA OF chicken and pork) [9,114-117]. These cases were included in TRAVELER the Table 1. Considering the several Gnathostoma species can cause human infection, we indicated the species names only To collect the fish-borne nematodiases cases reported in the when the surgically removed specimens were identified by literature, an extensive internet electronic search was conduct- morphological and/or molecular examination, because im- ed using appropriate key-words, like nematode human infec- mune-serological methods alone do not always provide defi- tions, emerging diseases, neglected diseases, anisakiasis, gna- nite evidence of species identification due to strong cross-reac- thostomiasis, capillariasis, sushi, sashimi, ceviche, traveler dis- tion of antibody beyond the species [118-120]. Therefore, even eases, Gnathostoma, Pseudoterranova, Anisakis, Capillaria, etc., as when the causative species were identified by serological tools, well as various combinations of these key-words. The internet we referred to as Gnathostoma sp. within the Table 1 and the search engines, PubMed, Medline, Google and Google Scholar corresponding presumptive species is indicated in brackets. were used, and the references of every paper were verified in order to identify useful and reliable publications. We recog- FISH-BORNE NEMATODIASES AMONG nized it is practically impossible to track all the available litera- TRAVELERS ture, but it is hoped that nearly all the cases reported were tracked. The number of infection cases of returned travelers, parasite For the purposes of this study we consider a returned travel- species, country of origin, country where the infection was pre- er as a traveler who had been abroad for a period no longer sumably acquired, and references are indicated in Table 1. than 6 months before returning to the original country. There- According to the data collected, 100 cases of fish-borne fore, people who lived several years abroad and returned in- nematode infections have been reported in returned travelers fected to the original country [74,76-78,99-101] were not con- in 22 countries, namely, Argentina, Austria, Australia, Belgium, sidered as travelers. People who immigrated to other countries Brazil, Canada, England, France, Germany, Israel, Italy, Japan, and developed there the disease [13,102-110] were not consid- Korea, Laos, Peru, , Spain, Switzerland, Thailand, ered as travelers either. Moore et al. [111] referred 12 persons Taiwan, the Netherlands, USA and Venezuela. The causative infected with Gnathostoma, who were examined in the Hospi- nematode species were Angiostrongylus cantonensis (1 case), Ani- tal for Tropical Diseases, in London. The patients were origi- sakis simplex (6 cases in total), Capillaria philippinensis (8), Gna- nal, or visited a number of countries (China, South Korea, thostoma malaysiae (2), G. spinigerum (3), G. binucleatum? (7), G. Bangladesh, India, Thailand, SE Asia, Vietnam, Thailand, etc.) doloresi? (1), G. spinigerum? (27) and Gnathostoma sp. (46). where gnathostomiasis is frequent, and some reported to have eaten raw fish. Some of the patients were immigrants, but the DISCUSSION number of travelers or immigrants in their study is not clear, and the duration of the visits in the case of travelers was not In this review, surprisingly gnathostomiasis is the most fre- Eiras et al.: Fish-borne nematodiases among returned travelers 219

Table 1. Cases of infection with fish-borne nematodes among returned travelers

Parasite From To No. of cases Reference Angiostrongylus cantonensis Tahiti France 1 [15,38] “Anisakiasis” Not indicated Australia 2 [34,121] “Anisakiasis” Chile Belgium 1 [122] “Anisakisasis” Belgium Israel 1 [123] Anisakis simplex USA Austria 2 [124] Capillaria philippinensis Indonesia Italy 1 [5] C. philippinensis Saipan island Korea 1 [77] C. philippinensis Phillipines & Thai Taiwan 1 [68] C. philippinensis Phillipines Taiwan 1 [68] C. philippinensis Thailand Taiwan 3 [125] C. philippinensis Malaysia/Singapore Japan 1 [71] Gnathostoma malaysiae Myanmar Japan 1-2 [126] G. spinigerum Vietnam Japan 1 [115] G. spinigerum Philippines USA 1 [127] G. spinigerum Thailand USA 1 [128] Gnathostoma sp. (G. binucleatum ?) Brazil or Colombia? Belgium 1 [129] Gnathostoma sp. (G. binucleatum ?) Peru Brazil 1 [130] Gnathostoma sp. (G. binucleatum ?) USA Colombia 1 [131] Gnathostoma sp. (G. binucleatum ?) Mexico USA 1 [132] Gnathostoma sp. (G. binucleatum ?) Mexico France 1 [7] Gnathostoma sp. (G. binucleatum ?) Mexico Spain 1 [133] Gnathostoma sp. (G. binucleatum ?) Peru Switzerland 1 [6] Gnathostoma sp. (G. doloresi ?) Sri Lanka Korea 1 [134] Gnathostoma sp. (G. spinigerum ?) China Australia 15 [135]a Gnathostoma sp. (G. spinigerum ?) Thailand Canada 1 [14] Gnathostoma sp. (G. spinigerum ?) Hungary France 1 [136] Gnathostoma sp. (G. spinigerum ?) Germany 1 [137] Gnathostoma sp. (G. spinigerum ?) Thailand Germany 1 [138] Gnathostoma sp. (G. spinigerum ?) Laos Germany 1 [8] Gnathostoma sp. (G. spinigerum ?) Peru Germany 1 [139] Gnathostoma sp. (G. spinigerum ?) Thailand or Indonesia Spain 1 [140] Gnathostoma sp. (G. spinigerum ?) Thailand Spain 1 [133] Gnathostoma sp. (G. spinigerum ?) Vietnam Switzerland 1 [141] Gnathostoma sp. (G. spinigerum ?) Southeast Asia The Netherlands 2 [142] Gnathostoma sp. (G. spinigerum ?) Thailand or Indonesia Switzerland 1 [143] Gnathostoma sp.b Colombia Argentina 1 [10] Gnathostoma sp. Vietnam Korea 1 [9] Gnathostoma sp. Botswana England 2 [144] Gnathostoma sp. Thailand or Myanmar Austria 1 [117] Gnathostoma sp. Borneo England 1 [111] Gnathostoma sp.c Cambodia France 3 [145] Gnathostoma sp.c Thailand France 1 [145] Gnathostoma sp.c Vietnam France 1 [145] Gnathostoma sp. Brazil France 1 [146] Gnathostoma sp. Cambodia France 2 [147] Gnathostoma sp. Laos France 2 [147] Gnathostoma sp. China France 2 [147] Gnathostoma sp. Myanmar France 1 [147] Gnathostoma sp. Japan France 2 [147,148] Gnathostoma sp. Sri Lanka France 1 [147] Gnathostoma sp. Thailand France 1 [147] Gnathostoma sp. Vietnam France 2 [147,149] Gnathostoma sp. Mexico France 2 [147] Gnathostoma sp. Bali France 1 [148] Gnathostoma sp. Brazil Japan 1 [16]d Gnathostoma sp. South Africa Japan 1 [16]d Gnathostoma sp. Cambodia Japan 1 [16]d Gnathostoma sp. USA Venezuela 1 [24] Gnathostoma sp. Ecuador Peru 1 [150] Gnathostoma sp. “Caribbean” Peru 1 [150] Gnathostoma sp. China Spain 2 [111] Gnathostoma sp. Zambia South Africa 1 [151] Gnathostoma sp. Botswana South Africa 1 [152] Gnathostoma sp. Tanzania USA 3 [153] Gnathostoma sp. Vietnam USA 1 [114] Gnathostoma sp. Zambia USA 1 [151] Gnathostoma sp. Turkey or Thailand USA 1 [13] Gnathostoma sp. Thailand USA 1 [154] aA personal communication from A. Fuller in Reference [135]. bThis case was reported without immunodiagnosis and the validity of the description was questioned by Joob and Wiwanitkit [155], and the same case was commented by Rodríguez-Morales et al. [156]. See replies by Orduna et al. [157,158]. cMénard et al. [145] reported from one of the patients identified by histological observation. However, the country where the traveler came from was not indicated. dUnpublished data from Y. Nawa in Reference [16]. 220 Korean J Parasitol Vol. 56, No. 3: 215-227, June 2018

quent fish-borne nematodiasis among global travelers, where- any other fish-borne nematodiasis is the underestimation due as the number of anisakidosis cases was extremely low in spite to in accurate diagnosis. It may be questioned the validity of of its high incidence in some countries like Japan. One simple the number of fish-borne nematodiasis cases described so far and most possible explanation for this difference is due to the in returned travelers. In some countries like Australia, where difference of of the diseases. Generally, a the popularity of consuming raw or undercooked fish is great, few days to few months are required for the development of there is only one case report of human infection [34]. Shamsi clinical manifestations of gnathostomiasis after the infective [121] explained that probably anisakidosis is underestimated larvae in uncooked fish were ingested [84,85]. Thus, travelers in the country due to the sometimes difficulty to diagnose of with peculiar of gnathostomiasis will visit infection, and suspected the presence of more hidden cases in clinicians after they have returned their home country where the country. Verhame and Ramboer [122] considered also that clinicians are not familiar with such a strange disease. In con- the disease is underestimated in Belgium and in most other trast, the vast majority of anisakidosis patients develop their European countries. According to these authors, “It seems like- signs and symptoms of acute within few hours after ly that only the tip of the iceberg is seen and that many of the ingestion of the larvae in “Sushi”, “Sashimi” etc. during their less severe cases remain under-diagnosed, the condition being travel and are treated immediately by endoscopic specialists. considered transient gastroenteritis”. As reported by Sakanari In endemic countries like Japan, anisakiasis cases of travelers and McKerrow [162], the disease is often misdiagnosed and, from overseas might thus not appear as case reports because in a clinicopathological study of 92 cases of anisakiasis in Ja- the disease is so common. pan, “over 60% of cases were diagnosed preoperatively as ap- As an alternative explanation of extremely low incidence of pendicitis, acute abdomen, gastric tumour or cancer, ileitis, anisakidosis among international travelers, the responsible cholecystitis, diverticulitis, tuberculous peritonitis, and cancer species and the sources of fish used for “Sushi” and “Sashimi” of the pancreas”. Therefore, the number of cases of anisakiasis in restaurants should be considered. According to Nawa et al. in returned traveler may be in fact much higher than the few [12], fish which are preferentially served in qualified Japanese cases reported so far. restaurants are less contaminated or even free of Anisakis. As can be seen in Table 1, the number of gnathostomiasis However, some less expensive marine fish like mackerel and cases among travelers is unexpectedly high compared with mollusks like squid, which are also often used for “Sushi” and other fish-borne nematodiasis. This unexpected result is, as “Sashimi” in cheap local restaurants, are many times heavily has been discussed above, at least in part attributed to the na- infected with Anisakis and the risk of infection is higher. Salm- ture of pathogenesis of Gnathostoma larvae. Different from ani- on is the fish species most commonly used for “Sushi” and sakid larvae in the stomach to cause extra-rapid clinical mani- “Sashimi” worldwide, and the large part of salmon are origi- festation, usually several days to months are required for Gna- nated in aquaculture net cages facilities where they are inten- thostoma larvae after being ingested to cause clinical symptoms sively fed with processed feeds. A number of studies showed in humans. Thus, the disease mostly developed after returning that such fish are free from Anisakis simplex, although some from the travel and it is difficult for patients to link the disease specimens may be infected through the consumption of con- with their experience of having ethnic dishes. Together with taminated small invertebrates and fish, which can enter the rapid movement of the skin lesions, unknown causes of the net cages. It was demonstrated that the proportion of infected disease often terrify the patients. fish in the farmed species is extremely low [159-161], and this While reviewing gnathostomiasis cases among travelers, we fact may probably contribute decisively for the surprisingly recognized that some Gnathostoma species identifications may low prevalence of anisakidosis in returned travelers. However, not be accurate because, in many of the cases, they were diag- low anisakiasis infection in farmed fish does not necessarily nosed based on clinical features and the results of serodiagno- means low prevalence infection rates in humans eating this sis, but not based upon the morphological and/or molecular kind of food-an evaluation of the amount of food ingested observation of the worms. Even when worms were obtained would be necessary to integrate all the facts involved in the hu- from patients, it is extremely difficult to distinguish G. spinige- man infection by Anisakis spp. rum and G. binucleatum from each other. In fact, many misdi- Another explanation for low incidence of anisakidosis or agnosis of G. binucleatum as G. spinigerum have been reported Eiras et al.: Fish-borne nematodiases among returned travelers 221

until recent development of molecular identification [84,85]. ate or paratenic hosts. In this literature survey, we found 2 ref- Because those 2 species distribute geographically different erences [38,164] mentioning about travelers of possible infec- places, travel history of the patients is helpful to speculate the tion with A. cantonensis. In 1 case (Southeast Pacific to USA) causative species [84,85]. Since the chance of detection of [164], the patient was serologically diagnosed as eosinophilic worms in surgical specimen is extremely low and the immu- due to A. cantonensis infection. Although the pa- nodiagnositic tools are not sensitive enough for identification tient ate seafoods, he has no clear history of ingesting snail in- of causative pathogen at the species level, development of termediate hosts or other possible source of infection [164]. In more specific (and of course sensitive) diagnostic methods is another case (Tahiti to France), the patient has a history of eat- awaited. ing raw fish, which is considered as the source of infection Intestinal capillariasis caused by a nematode, Capillaria phil- [38], so that this case is included in our list (Table 1). Howev- ippinensis, is rather a rare but famous fish-borne nematodiasis er, in the latter case, possible infection by eating shrimp, vege- because of its high mortality. Due to auto-infection, delayed tables or any other kind of contaminated food materials can- diagnosis/treatment often resulted in death due to protein-los- not be ruled out. High prevalence of A. cantonensis larvae in ing gastroenteropathy. After the discovery of its first outbreak shrimp in Tahiti has been reported [165]. In terms of importa- in the northern Ruzon of the Philippines in the 1960s [21,22], tion of A. cantonensis from non-endemic to endemic areas, a its endemic areas have expanded to Thailand [64], Egypt [66] possible role of rodents traveling on cargo ships is evident by and Taiwan [67,68]. Various species of freshwater or brackish molecular identification of the geographical isolates of A. can- water fish play a role of the intermediate hosts, the source of tonensis [166]. human infection, and human infection occurs after ingesting Finally, in this review, we were unable to find any report of raw or undercooked fish. As shown in Table 1, capillariasis is traveler’s infections with Hysterothylacium spp., Contracaecum rather a rare disease among travelers – just 8 cases, and all of spp., Eustrongylides spp., or although these them have a history of consuming raw fish. One of the reasons are known as zoonotic fish-borne nematodes with records of for this low incidence might be because the endemic areas are human cases [32-36]. This is not surprising because human generally remote from the common tourism areas. However, it infections with these nematode species in general are extreme- should be noted that the establishment of C. philippinensis in ly rare and only few cases have been recorded sporadically the new endemic locality has been caused by migration of in- worldwide. The infection chance of travelers with these species fected people from an endemic area. Such an example was is supposed to be highly limited. seen in Pudoc West and several other regions in the Philip- In conclusion, this is the first extensive literature review on pines [21]. Lu et al. [68] suggested the possibility of some of fish-borne nematodiasis among travelers. The results showed the about 200,000 foreign laborers in Taiwan who originated unexpectedly high incidence of gnathostomiasis and low inci- from major epidemic areas might contribute to the spread of dence of anisakidosis. This discrepancy seems to be due pri- the disease in Taiwan. Although the emergence of intestinal marily to the difference of the incubation period of the diseas- capillariasis in Egypt is often considered to be due to large es. Other possibilities are also discussed. number of migrant labors from the endemic areas, the exact Many countries where the fish-borne nematodiases exists, a reasons still remain obscure [163]. These observations suggest variety of popular dishes containing raw fish, as well as the that the disease transmission by immigrants is much more im- high number of fish species infected were used in the confec- portant than by travellers for the epidemiology of C. philippi- tion of ethnic dishes of raw fish. This may be one of the rea- nensis infection in humans. sons for the relatively large variety of cases in returned travelers Although Angiostrongylus cantonensis is principally not a fish- (infected in 30 countries for travelers belonging to 22 coun- borne nematode parasite, its intermediate snail hosts are the tries). In terms of clinical manifestation, most of fish-borne main source of causing human infections and are often sold nematodiases listed in this review have unique signs and in fish markets. Humans may contract the infection by ingest- symptoms. Even so, most of atypical forms are probably un- ing infected snails or paratenic hosts like prawns, crabs and der-diagnosed [111,149]. frogs, and may be also by consuming vegetables contaminated In general, only few clinicians and laboratory workers in with larvae from the degenerated/crashed body of intermedi- non-endemic areas are familiar with these diseases [11,74] and 222 Korean J Parasitol Vol. 56, No. 3: 215-227, June 2018

most clinicians have difficulties in recognizing the symptoms 47: 10-12. of the infections [110,167]. Early diagnosis of the infection is 6. Chappuis F, Farinelli T, Loutan L. treatment of a traveler who returned from Peru with cutaneous gnathostomia- important because in cases of Capillaria philippinensis infection, sis. Clin Infect Dis 2001; 33: e17-e19. delay in diagnosis can cause severe life threatening disease 7. Del Giudice P, Dellamonica P, Durant J, Rahelinrina V, Gro- with high mortality rates [125]. According to Lu et al. [68], de- busch MP, Janitschke K, Dahan-Guedj A, Le Fichoux Y. A case layed diagnosis of capillariasis for more than a year was re- of gnathostomiasis in a European traveler returning from Mex- ported from Japan, Korea, Egypt and India. ico. Br J Dermatol 2001; 145: 487-489. In summary, we can conclude that 8. Hennies F, Jappe U, Kapaun A, Enk A. Gnathostomiasis: im- port from Laos. J Dtsch Dermatol Ges 2006; 4: 414-416. 1. The consumption of raw, alive, or undercooked fish, both 9. Yang JH, Kim M, Kim ES, Na BK, Yu SY, Kwak HW. Imported marine and freshwater, may originate travelers infection intraocular gnathostomiasis with subretinal tracks confirmed caused by zoonotic fish-borne nematodes belonging to by western blot assay. Korean J Parasitol 2012; 50: 73-78. different species. 10. Orduna TA, Lloveras SC, Echazarreta SE, Garro SL, González 2. Returned travelers may constitute a mean of spreading the GD, Falcone CC. Dermatosis de origen alimentário al regresso parasites in countries where the parasites did not exist. de un viaje: gnathostomiasis. Medicina (B Aires) 2013; 73: 558- 561 (in Spanish). 3. Physicians and health authorities must advice travelers on 11. Herman JS, Chiodini PL. Gnathostomiasis, another emerging the dangers of risk behaviors in order to not acquire the imported disease. Clin Microbiol Rev 2009; 22: 484-492. infection. 12. Nawa Y, Hatz C, Blum J. Sushi delights and parasites: the risk of fishborne and foodborne parasitic zoonoses in Asia. Clin ACKNOWLEDGMENTS Infect Dis 2005; 41: 1297-1303. 13. Rusnak JM, Lucey DR. Clinical gnathostomiasis: case report and review of the English-language literature. Clin Infect Dis The authors acknowledge colleagues who helped with the 1993; 16: 33-50. literature survey: Lo Re, Masahide Yoshikawa, Mortada H.F. El- 14. Houston S. Gnathostomiasis: report of a case and brief review. Shabrawi, O. Bjelić-Čabrilo, Paron Dekumyoy, Patricio Torres, Can J Infect Dis 1994; 5: 125-129. V. Stéphane Ranque. This paper was supported by MEC/MCTI/ 15. Clément-Rigolet MC, Danis M, Caumes E. La gnathostomose, CAPES/CNPq/FAPS. Participation of JC Eiras was supported une maladie exotique de plus en plus souvent importée dans les pays occidentaux. Presse Medi 2004; 33: 1527-1532 (in by the Portuguese Foundation for Science and Technology French). (FCT), Project UID/Multi/04423/2013, and by Cesumar (Cen- 16. Nawa Y, Nakamura-Uchiyama F. An overview of gnathostomia- tro Universitario Cesumar, Brasil). sis in the world. Asian J Trop Med Public Health 2004; 35 (suppl): 87-91. CONFLICT OF INTEREST 17. Ligon BL. Gnathostomiasis: a review of a previously localized zoonosis now crossing numerous geographical boundaries. Se- min Pediatr Infect Dis 2005; 16: 137-143. The authors declare they have not conflict of interest. 18. Nawa Y, Katchanov J, Yoshikawa M, Rojekittikhun W, Decu- myoy P, Kusolusuk T, Watanakulpanich D. Ocular gnathosto- REFERENCES miasis: a comprehensive review. J Trop Med Parasitol 2010; 33: 77-86. 1. UNWTO. UNWTO annual report 2016. [Internet]; Available 19. Katchanov J, Sawanyawisuth K, Chotmongkol V, Nawa Y. Neu- from: http://media.unwto.org/publication/unwto-annual-re- rognathostomiasis, a neglected parasitosis of the central ner- port-2016. vous system. Emerg Infect Dis 2011; 17: 1174-1180. 2. McCarthy J, Moore TA. Emerging helminth zoonoses. Int J Par- 20. Diaz JH. Gnathostomiasis: an emerging infection of raw fish asitol 2000; 30: 1351-1360. consumers in Gnathostoma nematode-endemic and nonen- 3. Ryan ET, Wilson ME, Kain KC. Illness after international travel. demic countries. J Travel Med 2015; 22: 328-324. N Engl J Med 2002; 347: 505-516. 21. Cross JH, Belizario V. Capillariasis. In Murrell KD, Fried B eds, 4. Steffen R, deBernardis C, Baños A. Travel epidemiology--a Food Borne Parasitic Zoonoses. New York, USA. Springer Sci- global perspective. Int J Antimicrob Agents 2003; 21: 89-95. ence & Business Media. 2007, pp 209-234. 5. Chichino G, Bernuzzi AM, Bruno A, Cevini C, Atzori C, Malfita- 22. Cross JH. Intestinal capillariasis. Clin Microbiol Rev 1992; 5: no A, Scaglia M. Intestinal capillariasis (Capillaria philippinensis) 120-129. acquired in Indonesia: A case report. Am J Trop Med Hyg 1992; 23. Lamothe Argumedo R. Gnatostomiasis ocular humana. Casos Eiras et al.: Fish-borne nematodiases among returned travelers 223

registrados en todo el mundo entre 1937 y 2005. Rev Mex 40. Macpherson CN. Human behaviour and the epidemiology of Oftalmol 2006; 80: 185-190 (in Spanish). parasitic zoonoses. Int J Parasitol 2005; 35: 1319-1331. 24. Nawa Y, Yoshikawa M, Sawanyawisuth K, Chotmongkol V, 41. Broglia A, Kapel C. Changing dietary habits in a changing Figueiras SF, Benavides M, Camacho SPD. Ocular gnathosto- world: emerging drivers for the transmission of foodborne par- miasis-update of earlier survey. Am J Trop Med Hyg 2017; 97: asitic zoonoses. Vet Parasitol 2011; 182: 2-13. 1232-1234. 42. Conlan JV, Sripa B, Attwood S, Newton PN. A review of para- 25. Chai JY, Darwin Murrell K, Lymbery AJ. Fish-borne parasitic sitic zoonoses in a changing Southeast Asia. Vet Parasitol 2011; zoonoses: status and issues. Int J Parasitol 2005; 35: 1233- 182: 22-40. 1254. 43. Torgerson PR, Macpherson CN. The socioeconomic burden of 26. Murrell KD, Fried B eds. Food Borne Parasitic Zoonoses: Fish parasitic zoonoses: global trends. Vet Parasitol 2011; 182: 79- and Plant-Borne Parasites. New York, USA. Springer Science & 95. Business Media, 2007. 44. Nyindo M, Lukambagire AH. Food-borne zoonotic trema- 27. Robinson MW, & Dalton JP. Zoonotic helminth infections with todes: devious old flukes in an urbanized, global village. Patho- particular emphasis on and other trematodiases. gen Infect Dis 2016; 1: e1187. Philos Trans R Soc Lond B Biol Sci 2009; 364: 2763-2776. 45. Hochberg NS, Hamer DH, Hughes JM, Wilson ME. Anisakido- 28. Toledo R, Esteban JG, Fried B. Current status of food-borne sis: perils of the deep. Clin Infect Dis 2010; 51: 806-812. trematode infections. Eur J Clin Microbiol Infect Dis 2012; 31: 46. Audicana MT, Kennedy MW. Anisakis simplex: from obscure in- 1705-1718. fectious worm to inducer of immune hypersensitivity. Clin Mi- 29. Hung NM1, Madsen H, Fried B. Global status of fish-borne crobiol Rev 2008; 21: 360-379. zoonotic trematodiasis in humans. Acta parasitol 2013; 58: 47. Lim H, Jung BK, Cho J, Yooyen T, Shin EH, Chai JY. Molecular 231-258. diagnosis of cause of anisakiasis in humans, South Korea. 30. Couture C, Measures L, Gagnon J, Desbiens C. Human intesti- Emerg Infect Dis. 2015; 21: 342-344. nal anisakiosis due to consumption of raw salmon. Am J Surg 48. Sohn WM, Na BK, Kim TH, Park TJ. Anisakiasis: report of 15 Pathol 2003; 27: 1167-1172. gastric cases caused by Anisakis type I larvae and a brief review 31. Torres P, Jercic MI, Weitz JC, Dobrew EK, Mercado RA. Human of Korean anisakiasis cases. Korean J Parasitol 2015; 53: 465- pseudoterranovosis, an emerging infection in Chile. J Parasitol 470. 2007; 93: 440-443. 49. Sohn WM, Kang JM, Na BK. Molecular analysis of Anisakis type 32. Yagi K, Nagasawa K, Nakagawa A, Sato N, Kikuchi K, Ishikura H. I larvae in marine fish from three different sea areas in Korea. Female worm Hysterothylacium aduncum excreted from human: Korean J Parasitol 2014; 52: 383-389. a case report. Jpn J Parasitol 1996; 45: 12-23. 50. Fukita Y, Asaki T, Katakura Y. Some like it raw: an unwanted re- 33. González-Amores Y, Clavijo-Frutos E, Salas-Casanova C, Al- sult of a sushi meal. Gastroenterology 2014; 146: e8-e9. cain-Martínez G. Direct parasitological diagnosis of infection 51. Imataki O, Bandoh S, Kawakami K, Uemura M. The leading with Hysterothylacium aduncum in a patient with epigastralgia. seafood cuisine of anisakidosis in Japan. Clin Infect Dis 2016; Rev Esp Enferm Dig 2015; 107: 699-700. 62: 1612-1613. 34. Shamsi S, Butcher AR. First report of human anisakidosis in 52. Kapral C, Haditsch M, Wewalka F, Schatzlmayr W, Lenz K, Auer Australia. Med J Aust 2011; 194: 199-200. H. The first case of anisakiasis acquired in Austria. Z Gastroen- 35. Eberhard ML, Ruiz-Tiben E. Cutaneous emergence of Eustron- terol 2009; 47: 1059-1061 (in German). gylides in two persons from South Sudan. Am J Trop Med Hyg 53. da Cruz AR, de Sousa Souto PC, Ferrari CKB, Allegretti SM, Ar- 2014; 90: 315-317. rais-Silva WW. Endoscopic imaging of the first clinical case of 36. Agrawal R, Kumar P, Mishra PR, Gupta R, Premi HK. Dioctophy- anisakidosis in Brazil. Sci Parasitol 2010; 11: 97-100. ma renale: a chance finding on bladder catheterisation of a 54. Plath F, Holle A, Zendeh D, Möller FW, Barten M, Reisinger EC, pregnant female. Indian J Med Case Reports 2014; 3: 70-72. Liebe S. Anisakiasis of the stomach--a case report from Germa- 37. Cowie RH. Pathways for transmission of and ny. Z Gastroenterol 2001; 39: 177-180 (in German). the risk of disease associated with them. Hawaii J Med Public 55. Shin EH, Guk SM, Kim HJ, Lee SH, Chai JY. Trends in parasitic Health 2013; 72(Suppl): 70-74. diseases in the Republic of Korea. Trends Parasitol 2008; 24: 38. Thobois S, Broussolle E, Aimard G, Chazot G. Ingestion of raw 143-150. fish: a cause of eosinophilic meningitis caused by Angiostrongy- 56. Cha HJ, Ock MS. Anisakidosis in Korea; Changes over the last lus cantonensis after a trip to Tahiti. Presse Medi 1996; 25: 508 decade. Kosin Med J 2012; 27: 73-78. (in French). 57. Mercado R, Torres P, Muñoz V, Apt W. Human infection by Pseu- 39. Grundy-Warr C, Andrews RH, Sithithaworn P, Petney TN, Sripa doterranova decipiens (Nematoda, Anisakidae) in Chile: report of B, Laithavewat L, Ziegler AD. Raw attitudes, wetland cultures, seven cases. Mem Inst Oswaldo Cruz 2001; 96: 653-655. life-cycles: socio-cultural dynamics relating to Opisthorchis viver- 58. Torres P, Jercic MI, Weitz JC, Dobrew EK, Mercado RA. Human rini in the Mekong Basin. Parasitol Int 2012; 61: 65-70. pseudoterranovosis, an emerging infection in Chile. J Parasitol 224 Korean J Parasitol Vol. 56, No. 3: 215-227, June 2018

2007; 93: 440-443. Korean J Parasitol 1994; 31: 43-48. 59. Weitzel T, Sugiyama H, Yamasaki H, Ramirez C, Rosas R, Mer- 75. Jung WT, Kim HJ, Min HJ, Ha CY, Kim HJ, Ko GH, Na BK, cado R. Human infections with Pseudoterranova cattani nema- Sohn WM. An indigenous case of intestinal capillariasis with todes, Chile. Emerg Infect Dis 2015; 21: 1874. protein-losing enteropathy in Korea. Korean J Parasitol 2012; 60. Cabrera R, Luna-Pineda MA, Suárez-Ognio L. New case of hu- 50: 333-337. man infection by a Pseudoterranova decipiens larva (Nematode, 76. Kwon Y, Jung HY, Ha HK, Lee I. An imported case of intestinal Anisakidae) in Peru. Rev Gastroenterol Peru 2003; 23: 217-220 capillariasis presenting as protein-losing enteropathy Korean J (in Spanish). Pathol 2000; 34: 235-238 (in Korean). 61. Cabrera R, Del Pilar M, Altamirano T. Anisakidosis a marine 77. Lee SH, Rhee PL, Lee JH, Lee KT, Le JK, Sim SG, Lee SK, Kim JJ, parasitic zoonosis: unknown or emerging in Peru? Rev Gastro- Ko KC, Paik SW, Rhee JC, Choi KW, Lee NY, Cho SL, Ryu KH. A enterol Peru 2004; 24: 335-342 (in Spanish). case of intestinal capillariasis: fourth case report in Korea. Kore- 62. Daschner A, Cuéllar C, Rodero M. The Anisakis allergy debate: an J Gastroenterol 1999; 34: 542-546 (in Korean). does an evolutionary approach help? Trends Parasitol 2012; 78. Ha M, Jun DH, Kim JH, Kim YJ, Kwon KA, Park DK, Ku YS. In- 28: 9-15. testinal capillariasis diagnosed by endoscopic biopsy. Clin En- 63. Mattiucci S, Fazii P, De Rosa A, Paoletti M, Megna AS, Glielmo A, dosc 2013; 46: 675-678. De Angelis M, Costa A, Meucci C, Calvaruso V, Sorrentini I, 79. Soukhathammavong P, Sayasone S, Harimanana AN, Akkha- Palma G, Bruschi F, Nascetti G. Anisakiasis and gastroallergic vong A, Thammasack S, Phoumindr N, Choumlivong K, reactions associated with Anisakis pegreffii infection, Italy. Emerg Choumlivong K, Keoluangkhot V, Phongmany S, Akkhavong Infect Dis 2013; 19: 496-499. K, Hatz C, Strobel M, Odermatt P. Three cases of intestinal ca- 64. Saichua P, Nithikathkul C, Kaewpitoon N. Human intestinal pillariasis in Lao People’s Democratic Republic. Am J Trop Med capillariasis in Thailand. World J Gastroenterol 2008; 14: 506- Hyg 2008; 79: 735-738. 510. 80. Hoghooghi-Rad N, Maraghi S, Narenj-Zadeh A. Capillaria phil- 65. Youssef FG, Mikhail EM, Mansour NS. Intestinal capillariasis in ippinensis infection in Khoozestan Province, Iran: case report. Egypt: a case report. Am J Trop Med Hyg 1989; 40: 195-196. Am J Trop Med Hyg 1987; 37: 135-137. 66. Attia RA, Tolba ME, Yones DA, Bakir HY, Eldeek HE, Kamel S. 81. el Hassan EH, Mikhail WE. Malabsorption due to Capillaria Capillaria philippinensis in Upper Egypt: has it become endemic? philippinensis in an Egyptian woman living in Dubai, United Am J Trop Med Hyg 2012; 86: 126-133. Arab Emirates. Trans R Soc Trop Med Hyg 1992; 86: 79. 67. Hwang KP. Human intestinal capillariasis (Capillaria philippi- 82. Dronda F, Chaves F, Sanz A, Lopez-Velez R. Human intestinal nensis) in Taiwan. Acta Paediatr Sinica 1998; 39: 82-85 (in Chi- capillariasis in an area of nonendemicity: case report and re- nese). view. Clin Infect Dis 1993; 17: 909-912. 68. Lu LA, Lin MR, Choi WM, Hwang KP, Hsu YH, Bair MJ, Liu JD, 83. Miyazaki I. On the genus Gnathostoma and human gnathosto- Wang TE, Liu TP, Chung WC. Human intestinal capillariasis miasis, with special reference to Japan. Exp Parasitol 1960; 9: (Capillaria philippinensis) in Taiwan. Am J Trop Med Hyg 2006; 338-370. 74: 810-813. 84. Waikagul J, Díaz-Camacho SP. Gnathostomiasis. In Murrell 69. Fan Z, Huang Y, Qian S, Lv G, Chen Y, Yang B, Zhong S, Lin G, KD, Fried B eds, Food-Borne Parasitic Zoonoses: Fish and Yan G. Serious diarrhea with weight loss caused by Capillaria Plant-Borne Parasites. New York, USA. Springer. 2007, pp 235- philippinensis acquired in China: a case report BMC Res Notes 261. 2012; 5: 554-557. 85. Nawa Y, Maleewong W, Intapan PM, Díaz-Camacho SP. Gna- 70. Vasantha PL, Girish N, Leela KS. Human intestinal capillariasis: thostoma. In Xiao L, Ryan U, Feng Y eds, Biology of Foodborne a rare case report from non-endemic area (Andhra Pradesh, In- Parasites. Boca Raton, USA. CRC Press. 2015, pp 405-425. dia). Indian J Med Microbiol 2012; 30: 236-239 86. Akahane H, Sano M, Kobayashi M. Three cases of human gna- 71. Sakoda H, Nakanishi T, Kishino B, Fushimi H, Kameyama M. thostomiasis caused by Gnathostoma hispidum, with particular Intestinal capillariasis infected in a Southeast Asian country -A reference to the identification of parasitic larvae. Southeast case report- Naika (Int Med) 1992; 69: 178-180 (in Japanese). Asian J Trop Med Public Health 1998; 29: 611-614. 72. Sakabe S, Fujinaga K, Tsuji N, Ito N, Umino A, Taniguchi M, 87. Subhedar V, Nandedkar S, Jain M, Bajpai T. Gnathostomiasis: a Mizutani M, Tamaki S, Tanigawa M, Tsuji K, Sato H. Marked rare case of cutaneous creeping eruptions. Indian J Dermatopa- hypoalbuminemia caused by Capillaria philippinensis. Nihon thol Diagn Dermatol 2014; 1: 32-34. Naika Gakkai Zasshi 2007; 96: 2282-2283 (in Japanese). 88. Pal M, Seid H, Giro B, Wakjira B, Abdo J. Gnathostomiasis - An 73. Lee SH, Hong ST, Chai JY, Kim WH, Kim YT, Song IS, Kim, SW, emerging nematodal zoonotic disease. Int J Livest Res 2013; 3: Choi BI, Cross JH. A case of intestinal capillariasis in the Re- 12-17. public of Korea. Am J Trop Med Hyg 1993; 48: 542-546. 89. Daengsvang S. Human gnathostomiasis in Siam with reference 74. Hong ST, Kim YT, Choe G, Min YI, Cho SH, Kim JK, Kook J, to the method of prevention. J Parasitol 1949; 35: 116-121. Chai JY, Lee SH. Two cases of intestinal capillariasis in Korea. 90. Eberhard ML. Dioctophymiasis and Eustrongylidiasis. In Con- Eiras et al.: Fish-borne nematodiases among returned travelers 225

nor DH, Chandler FW, Manz HJ, Schwartzl DA, Lacks EE eds, 2000; 4: 51-54. Pathology of Infectious Diseases. Stamford, USA. Appleton & 107. Qahtani F, Deschênes J, Ali-Khan Z, Maclean JD, Codère F, Lange. 1997. Mansour M, Burnier M Jr. Intraocular gnathostomiasis: a rare 91. Guerin PF, Marapendi S, MC GRAIL L. Intestinal perforation Canadian case. Can J Ophthalmol 2000; 35: 35-39. caused by larval Eustrongylides. Morb Mort Week Rep 1982; 31: 108. Lo Re V 3rd, Gluckman SJ. Eosinophilic meningitis due to Gna- 383-389. thostoma spinigerum. J Infect 2002; 45: 117-120. 92. Gunby P. One worm in the minnow equals too many in the 109. Germann R, Schachtele M, Nessler G, Seitz U, Kniehl E. Cere- gut. JAMA 1982; 248: 163. bral gnathostomiasis as a cause of an extended intracranial 93. Wittner M, Turner JW, Jacquette G, Ash LR, Salgo MP, Tanowitz bleeding. Klin Pediatr 2003; 215: 223-225. HB. Eustrongylidiasis: a parasitic infection acquired by eating 110. Claesson BA, Ulleryd P, Woxenius S, Chaicumpa W. Eosino- sushi. N Engl J Med 1989; 320: 1124-1126. philic meningitis due to Gnathostoma spinigerum in a Thai im- 94. Eberhard ML, Hurwitz H, Sun AM, Coletta D. Intestinal perfo- migrant in Sweden. Southeast Asian J Trop Med Public Health ration caused by larval Eustrongylides (Nematoda: Dioctophy- 2004; 35 (suppl): 104-106. matoidae) in New Jersey. Am J Trop Med Hyg 1989; 40: 648- 111. Moore DA, McCroddan J, Dekumyoy P, Chiodini PL. Gnathos- 650. tomiasis: an emerging imported disease. Emerg Infect Dis 95. Narr LL, O’Donnell JG, Libster B, Alessi P, Abraham D. Eu- 2003; 9: 647-650. strongylidiasis--a parasitic infection acquired by eating live 112. Ansart S, Perez L, Vergely O, Danis M, Bricaire F, Caumes E. Ill- minnow. J Am Osteopath Assoc 1996; 96: 400-402. nesses in travelers returning from the tropics: a prospective 96. Beaver PC, Theis JH. Diocytophymatid larval nematode in a study of 622 patients. J Travel Med 2005; 12: 312-318. subcutaneous from man in California. Am J Trop Med 113. Ansart S, Perez L, Jaureguiberry S, Danis M, Bricaire F, Caumes E. Hyg 1979; 28: 206-212. Spectrum of dermatoses in 165 travelers returning from the 97. Norouzi R, Manochehri A, Hanifi M. A case report of human tropics with skin diseases. Am J Trop Med Hyg 2007; 76: 184- infection with Dioctophyma renale from Iran. Urol J 2017; 14: 186. 3043-3045. 114. Crowley JJ, Kim YH. Cutaneous gnathostomiasis. J Am Acad 98. Katafigiotis I, Fragkiadis E, Pournaras C, Nonni A, Stravodimos Dermatol 1995; 33: 825-828. KG. A rare case of a 39 year old male with a parasite called Di- 115. Sakamoto M, Sato F, Mizuno Y, Komatsuzaki M, Yoshikawa K, octophyma renale mimicking renal cancer at the computed to- Yoshida M, Shiba K, Onodera S, Hosoya T, Kumagai M. Gna- mography of the right kidney. A case report. Parasito Int 2013; thostomiasis caused by Gnathostoma spinigerum etiologically di- 62: 459-460. agnosed upon extraction of the worm from the skin. Kansen- 99. Tokiwa T, Ueda W, Takatsuka S, Okawa K, Onodera M, Ohta N, shogaku Zasshi 2004; 78: 442-445 (in Japanese). Akao N. The first genetically confirmed case of Dioctophyme re- 116. Oliván-Gonzalvo G. Gnatostomiasis tras un viaje a China para nale (Nematoda: Dioctophymatida) in a patient with a subcu- realizar una adopción internacional. Med Clin (Barc.): 2006; taneous nodule. Parasitol Int 2014; 63:143-147. 19: 758-759 (in Spanish). 100. Develoux M, Dekumyoy P, Baygon E, Aractingi S. Imported 117. Schmutzhard E. Eosinophilic myelitis, a souvenir from South gnathostomiasis acquired in Myanmar. Med Mal Infect 2006; 6: East Asia. Pract Neurol 2007; 7: 48-51. 340-342 (in French). 118. Nopparatana C, Setasuban P, Chaicumpa W, Tapchaisri P. Puri- 101. Kim HS, Lee JJ, Joo M, Chang SH, Chi JG, Chai JY. Gnathostoma fication of Gnathostoma spinigerum specific antigen and immu- hispidum infection in a Korean man returning from China. Ko- nodiagnosis of human gnathostomiasis. Int J Parasitol 1991; rean J Parasitol 2010; 48: 259-261. 21: 677-687. 102. Nagler A, Pollack S, Hassoun G, Kerner H, Barzilai D, Lengy J. 119. Ishiwata K, Camacho SP, Ogata K, Nakamura-Uchiyama F, Hi- Human pleuropulmonary gnathostomiasis: a case report from romatsu K, Nawa Y. Evaluation of the antigenic similarities of Israel. Isr J Med Sci 1983; 19: 834-837. adult-worm extracts from three Gnathostoma species, using sera 103. Chabasse D, Cauchy AC, de Gentile L, Bouchara JP. Human from Mexican and Japanese patients with Gnathostoma infec- gnathostomiasis manifested by syn- tions. Ann Trop Med Parasitol 2003; 97: 629-637. drome. Apropos of a case. Bull Soc Pathol Exot Filiales 1988; 120. Neumayr A, Ollague J, Bravo F, Gotuzzo E, Jimenez P, Norton 81: 326-331. SA, Doanh PN, Nawa Y, Horii Y, Nickel B, Marti H. Cross-reac- 104. Dow C, Chiodini PL, Haines AJ, Michelson SM. Human gna- tivity pattern of Asian and American human Gnathostomiasis thostomiasis. J Infect 1988; 17: 147-149. in western blot assays using crude antigens prepared from Gna- 105. Lee SY, Hon ST, Chai JY. Description of a male Gnathostoma spi- thostoma spinigerum and Gnathostoma binucleatum third-stage nigerum recovered from a Thai woman with meningoeneepha- larvae. Am J Trop Med Hyg 2016; 95: 413-416. litis. Korean J Parasitol 1988; 26: 33-38. 121. Shamsi S. Recent advances in our knowledge of Australian ani- 106. Grobusch MP, Bergmann F, Teichmann D, Klein E. Cutaneous sakid nematodes. Int J Parasitol Parasites Wildl 2014; 3: 178- gnathostomiasis in a woman from Bangladesh. Int J Infect Dis 187. 226 Korean J Parasitol Vol. 56, No. 3: 215-227, June 2018

122. Verhamme MA, Ramboer CH. Anisakiasis caused by herring in German). vinegar: a little know medical problem. Gut 1988; 29: 843- 139. Bommer W. Excessive subcutaneous gnathostomosis after a six 847. months stay in Peru. Successful treatment with . 123. Berger S. Infectious Diseases of Israel-2011 Edition. Los Anger- Wien Klin Wochenschr 2004; 116 (suppl): 61-64 (in German). les, USA. GIDEON Information. 2011. 140. Puente S, Gárate T, Grobusch MP, Janitschke K, Bru F, Rodrí- 124. Auer H, Leskowschek H, Engler J, Leitner G, Wentzel C, Wolk- guez M, González-Lahoz JM. Two cases of imported gnathosto- erstorfer W, Schneider R. Epidemiologie und Nosologie der miasis in Spanish women. Eur J Clin Microbiol Infect Dis Anisakiose, einer in Mitteleuropa selten diagnostizierten Hel- 2002; 21: 617-620. minthozoonose–zwei Fallberichte. Wien Klin Wochenschr 141. Kunzle N, Laffitte E, De Heller HK, Landry P, Panizzon RG. In- 2007; 119 (suppl): 106-109 (in German). termittent cutaneous tumefaction after a trip to Vietnam. Ann 125. Bair MJ, Hwang KP, Wang TE, Liou TC, Lin SC, Kao CR, Wang Dermatol Venereol 2003; 130: 463-464 (in French). TY, Pang KK. Clinical features of human intestinal capillariasis 142. de Vries PJ, Kerst JM, Kortbeek LM. Migrating swellings from in Taiwan. World J Gastroenterol 2004; 10: 2391-2393 Asia: gnathostomiasis. Ned Tijdschr Geneeskd 2001; 145: 322- 126. Nomura Y, Nagakura K, Kagei N, Tsutsumi Y, Araki K, Suga- 325 (in Dutch). wara M. Gnathostomiasis possibly caused by Gnathostoma ma- 143. Elzi L, Decker M, Battegay M, Rutishauser J, Blum J. Chest laysiae. Tokai J Exp Clin Med 2000; 25: 1-6. after travel to the tropics. Lancet 2004; 363: 1198. 127. Tudor RC, Blair E. Gnathostoma spinigerum: an unusual cause of 144. Herman JS, Wall EC, van-Tulleken C, Godfrey-Faussett P, Bailey ocular nematodiasis in the western hemisphere. Am J Oph- RL, Chiodini PL. Gnathostomiasis acquired by British tourists thalmol 1971; 72: 185-190. in Botswana. Emerg Infect Dis 2009; 15: 594-597. 128. Raturi U, Burkhalter W. Gnathostomiasis externa: a case report. 145. Ménard A, Dos Santos G, Dekumyoy P, Ranque S, Delmont J, J Hand Surg AM 1986; 11: 751-753. Danis M, Bricaire F, Caumes E. Imported cutaneous gnathosto- 129. Theunissen C, Bottieau E, Van Gompel A, Siozopoulou V, miasis: report of five cases. Trans R Soc Trop Med Hyg 2003; Bradbury RS. Presumptive Gnathostoma binucleatum infection in 97: 200-202. a Belgian traveler returning from . Travel Med 146. Cornaglia J, Jean M, Bertrand K, Aumaître H, Roy M, Nickel B. Infect Dis 2016; 14: 170-171. Gnathostomiasis in Brazil: an emerging disease with a chal- 130. de Castro Dani CM, Mota KF, Sanchotene PV, Piñeiro-Maceira J, lenging diagnosis. J Travel Med 2016; 24: 1-4. Maia CPA. Gnatostomíase no Brasil – Relato de caso. An Brasil 147. Strady C, Dekumyoy P, Clement-Rigolet M, Danis M, Bricaire F, Dermatol 2009; 84: 400-404 (in Portuguese). Caumes E. Long-term follow-up of imported gnathostomiasis 131. Jurado LF, Palacios DM, López R, Baldión M, Matijasevic E. shows frequent treatment failure. Am J Trop Med Hyg 2009; Gnatostomiasis cutánea, primer caso confirmado en Colom- 80: 33-35. bia. Biomedica 2015; 35: 462-470 (in Spanish). 148. Vanahecke C, Perignon A, Monsel G, Regnier S, Paris L, Cau- 132. Funata M, Custis P, de la Cruz Z, de Juan E, Green WR. Intraoc- mes E. Aetiologies of creeping eruption: 78 cases. Br J Dermatol ular gnathostomiasis. Retina 1993; 13: 240-244. 2014; 170: 1166-1169. 133. Górgolas M, Santos-O'Connor F, Unzú AL, Fernández-Guerrero 149. Parola P, Bordmann G, Brouqui P, Delmont J. Eosinophilic ML, Gárate T, Troyas Guarch RM, Grobusch MP. Cutaneous pleural effusion in gnathostomiasis. Emerg Infect Dis 2004; 10: and medullar gnathostomiasis in travelers to Mexico and Thai- 1690-1691. land. J Travel Med 2003; 10: 358-361. 150. Villar de Cipriani E. Paniculitis migratoria eosinofílica en el 134. Bae EH, Koh BK, Kim JW. A case of human gnathostomiasis Perú: Gnathostoma como agente causal. Rev Peru Med Exp Salud successfully treated with Ivermectin. Ann Dermatol 2006; 18: Publica 2003; 20: 220-12. 33-36. 151. Hale DC, Blumberg L, Frean J. Case report: gnathostomiasis in 135. Hughes AJ, Biggs BA. Parasitic worms in the central nervous two travelers to Zambia. Am J Trop Med Hyg 2003; 68: 707- system: an Australian perspective. Internal Med J 2002; 32: 541- 709. 553. 152. Communicable Diseases Communiqué, November 2013, 12 136. Chandenier J, Husson J, Canaple S, Gondry-Jouet C, Deku- (www.nicd.ac.za/assets/files/Gnathostomiasis%20outbreak. myoy P, Danis M, Riveau G, Hennequin C, Rosa A, Raccurt CP. pdf). Medullary gnathostomiasis in a white patient: use of immuno- 153. Wolfe MS, Acosta AM, Lichtenfels JR, Neafie R, Ash LR. Gna- diagnosis and magnetic resonance imaging. Clin Infect Dis thostomiasis contracted in East Africa. Am J Trop Med Hyg, 2001; 32: e154-e157. 1996; 55: 120. 137. Slevogt H, Grobush MP, Suttorp N. Gnathostomiasis without 154. Stowens D, Simon G. Gnathostomiasis in Oneida County. NY led to a 5 year-delay in diagnosis. J Travel Med State J Med 1981; 81: 409-410. 2006; 10: 196. 155. Joob B, Wiwanitkit V. Gnathostomiasis after travelling. Medici- 138. Jelinek T, Ziegler M, Löscher T. Gnathostomiasis after a stay in na (Buenos Aires) 2014; 74: 263 (in Spanish). Thailand. Dtsch Med Wochenschr 1994; 119: 1618-1622 (in 156. Rodríguez-Morales AJ, Cárdenas-Giraldo EV, Manrique-Casta- Eiras et al.: Fish-borne nematodiases among returned travelers 227

ño S, Martínez-Pulgarín DF. Is there gnathostomiasis in Co- and its mysterious trip from Philippines to Egypt (review arti- lombia? Reflections from a possible case imported to Argenti- cle). J Egypt Soc Parasitol 2014; 44: 161-171. na. Medicina (B Aires) 2014; 74: 264 (in Spanish). 164. Ramirez-Avila L, Slome S, Schuster FL, Gavali S, Schantz PM, 157. Orduna TA, Lloveras SC, Echazarreta SE, Garro SL, González Sejvar J, Glaser CA. Eosinophilic meningitis due to Angiostron- GD, Falcone CC. In response: on a possible case of gnathosto- gylus and Gnathostoma species. Clin Infect Dis 2009; 48: 322- miasis. Medicina (B Aires). 2014; 74: 265 (in Spanish). 327. 158. Orduna TA, Lloveras SC, Echazarreta SE, Garro SL, González 165. Alicata JE, Brown RW. Observations on the method of human GD, Falcone CC. About a probable case of gnathostomiasis. infection with Angiostrongylus cantonensis in Tahiti. Can J Zool Medicina (B Aires), 2014; 74: 263-264 (in Spanish). 1962; 40: 755-760. 159. Marty GD. Anisakid larva in the viscera of a farmed Atlantic 166. Tokiwa T, Harunari T, Tanikawa T, Komatsu N, Koizumi N, salmon (Salmo salar). Aquaculture 2008; 279: 209-210. Tung KC, Suzuki J, Kadosaka T, Takada N, Kumagai T, Akao N, 160. Skov J, Kania PW, Olsen MM, Lauridsen JH, Buchmann K. Ohta N. Phylogenetic relationships of rat lungworm, Angio- Nematode infections of maricultured and wild in Dan- strongylus cantonensis, isolated from different geographical re- ish waters: a comparative study. Aquaculture 2009; 298: 24-28. gions revealed widespread multiple lineages. Parasitol Int 2012; 161. dos Santos CAML, Howgate P. Fishborne zoonotic parasites 61: 431-436. and aquaculture: a review. Aquaculture 2011; 318: 253-261. 167. Eiras JC, Pavanelli GC, Takemoto RM, Yamaguchi MU, Karkling 162. Sakanari JA, McKerrow JH. Anisakiasis. Clin Microbiol Rev LC, Nawa Y. Potential risk of fish-borne nematode infections in 1989; 2: 278-284. humans in Brazil–current status based on a literature review. 163. Khalifa R, Othman RA. Some studies on Capillaria philipinensis FAWPAR 2016; 5: 1-6.